Dental Caries and Growth in School-Age Children Heba A. Alkarimi, Richard G. Watt, Hynek Pikhart, Aubrey Sheiham and Georgios Tsakos Pediatrics 2014;133;e616; originally published online February 17, 2014; DOI: 10.1542/peds.2013-0846
The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/133/3/e616.full.html
PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
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Dental Caries and Growth in School-Age Children WHAT’S KNOWN ON THIS SUBJECT: There is conflicting evidence about the relationship between dental caries in primary teeth and children’s height and weight.
AUTHORS: Heba A. Alkarimi, MSc, PhD,a,b Richard G. Watt, MSc, PhD,b Hynek Pikhart, MSc, PhD,b Aubrey Sheiham, BDS, PhD,b and Georgios Tsakos, MSc, PhDb aKing
WHAT THIS STUDY ADDS: Findings reveal an inverse linear association between caries levels and children’s height and weight. The findings take the argument beyond the presence or absence of an association and provide a better understanding of the pattern of this association.
abstract BACKGROUND AND OBJECTIVE: Dental caries in young children is commonly untreated and represents a public health problem. Dental caries in children is reported to affect their anthropometric outcomes, but the evidence is conflicting. Some studies found no association, whereas others found that caries was associated with underweight or overweight. The objective was to assess the relationship between dental caries status and height and weight in 6- to 8-year-old Saudi children with high caries prevalence. METHODS: This study was a cross-sectional survey in schoolchildren aged 6 to 8 years attending military primary schools in Jeddah, Saudi Arabia. Caries status was assessed by using the dmft (decayed, missing, filled, teeth [primary teeth]) index. Height and weight were assessed by using z scores of height-for-age (HAZ), weight-for-age (WAZ), and BMI-for-age (BAZ) calculated by World Health Organization standardized procedures. Relationships between caries and HAZ, WAZ, and BAZ were assessed by using regression models. RESULTS: A total of 417 of the 436 eligible schoolchildren with complete data were included, with a response rate of 95.6%. Their mean dmft index was 5.7 6 4.2. There was an inverse linear relationship between caries status and children’s HAZ, WAZ, and BAZ and significantly lower anthropometric outcomes for children at each consecutive group with higher levels of caries. The associations remained significant after adjusting for dental, social, and demographic variables.
Fahad Armed Forces Hospital, Jeddah, Saudi Arabia; and Department of Epidemiology and Public Health University College London, London, United Kingdom bResearch
KEY WORDS height, weight, BMI, children, caries ABBREVIATIONS BAZ—BMI-for-age dmft—decayed, missing, filled, teeth (primary teeth) HAZ—height-for-age WAZ—weight-for-age WHO—World Health Organization Dr Alkarimi conceptualized and designed the study, carried out the analyses, and drafted the initial manuscript; Drs Watt and Sheiham conceptualized and designed the study and reviewed and revised the manuscript; Dr Pikhart contributed to the study design and data analysis and interpretation and reviewed and revised the manuscript; Dr Tsakos conceptualized and designed the study, contributed to data analysis and interpretation, and reviewed and revised the manuscript; and all authors approved the final manuscript as submitted. www.pediatrics.org/cgi/doi/10.1542/peds.2013-0846 doi:10.1542/peds.2013-0846 Accepted for publication Dec 17, 2013 Address correspondence to Heba Alkarimi, MSc, PhD, King Fahad Armed Forces Hospital (KFAFH), PO Box 54146, Jeddah, 21514, Saudi Arabia. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2014 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: Funded by the Saudi Ministry of Defense, King Fahad Armed Forces Hospital. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
CONCLUSIONS: The inverse linear association between dental caries and all anthropometric outcomes suggests that higher levels of untreated caries are associated with poorer growth in Saudi schoolchildren. Pediatrics 2014;133:e616–e623
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There is increased interest in the relationship between caries and growth in young children and mechanisms whereby caries may affect growth. Evidence linking caries in primary teeth and children’s anthropometric outcomes in cross-sectional studies is contradictory in terms of both the presence and the direction of the association. Some studies report a relationship between caries and poor growth.1–9 Two theories may explain this relationship (Fig 1). The first theory is that the direct impact of extensive untreated caries and associated pain and inflammation on the child’s ability to eat may result in undernutrition and growth impairment.1,10–14 The second theory includes the indirect effects of untreated caries and different body responses to chronic dental infection. Three mechanisms are suggested. The first concerns immune responses. Infected dental pulp may affect immunity and erythropoiesis,15–17 which may result in anemia18 and influence bone remodeling,19,20 sleep patterns,21,22 and food intake.23 This mechanism is supported by results of a randomized controlled trial showing that treatment of severe caries in children aged 6 to 7 years significantly improved their appetite.24 The second mechanism is related to endocrine responses. The interruption of slowwave sleep due to pain and infection may lead to impairment of growth hormone secretion.25 The third mechanism is linked to metabolic responses. Infections and related inflammation might result in micronutrient undernutrition through increasing energy expenditure and metabolic demands and impaired nutrient absorption.20 In contrast to the studies reporting a relationship between caries and poor growth, some studies did not find any relationship between anthropometric outcomes and caries26–29 or reported that caries is related to overweight.30–32
This inconsistency is also observed in findings from randomized controlled trials and nonrandom longitudinal studies.9,11,24,33–35 These inconsistent associations could be due to methodologic limitations, different caries definitions and detection methods, relying only on BMI, and using unadjusted formulas to calculate BMI rather than the age- and gender-adjusted World Health Organization (WHO)–recommended growth references.4,26,32,36–38 Another limitation is the failure to include the full range of BMI categories in the sample.37,38 In addition, most studies only focused on 1 direction of the association, either underweight or overweight, ignoring other possibilities.4,26,28,37–39 Interestingly, a recent systematic review showed a significant association between obesity and caries when BMIfor-age (BAZ) centiles were reported and nonsignificant findings when z scores or nonstandardized scales were reported.29 To date, no study has examined the relationship between caries and anthropometric outcomes in young children with high levels of untreated caries using height and weight as continuous variables and where no cutoff points for the diagnosis of underweight and overweight are used. Therefore, a study was conducted with the objective of assessing the nature of the relationship between different levels of caries and height and weight among 6- to 8-year-old Saudi schoolchildren. No assumptions were made on the direction of this association.
METHODS The sample consisted of all schoolchildren aged 6 to 8 years in the firstyear class (grade 1) of all military primary schools inJeddah, SaudiArabia. Children with parasitic infections at the time of the survey and children whose caregivers did not give consent were excluded. Children of military
personnel were selected because they had the highest prevalence of caries in Saudi Arabia.40 Parents were asked to complete a sociodemographic and health status questionnaire. A pilot study was conducted in 55 randomly selected children to test the feasibility of all clinical examinations. The research was approved, managed, and monitored by the Research and Ethics Committee of the King Fahad Armed Forces Hospital. Parental permission was obtained from the child’s legal caregivers. Measurements Anthropometric Measurements Anthropometric measurements were performed by using the Food and Nutrition Anthropometric Indictors Measurement Guide.41 A skilled nurse, blinded to the child’s dental status, carried out all anthropometric measurements. Measurements for height and weight were made to the nearest 0.1 cm and 0.1 kg, respectively. All anthropometric measures were performed in children without shoes and wearing light clothes. Height was measured by using a portable Harpenden pocket stadiometer (Chasmors Ltd, London, United Kingdom). Weight was measured by using a precalibrated digital Seca scale (model 767; Seca GmbH, Hamburg, Germany). All children were weighed at the same time of day (7:30–8:50 AM) and in the same relation to their eating time (before morning break). Three readings for both height and weight were taken for each child. The median of these readings was used for the analysis. Height and weight were assessed by using the z scores of height-for-age (HAZ), weight-for-age (WAZ), and BAZ.42 The calculation of z scores for height, weight, and BMI was based on the international reference standards for the assessment of nutritional status for a specific age and gender and were automatically
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FIGURE 1 Proposed mechanisms linking severe dental caries and dental pain and infections with height and weight in young children.
managed by using the WHO AnthroPlus software, which holds the WHO Reference 2007 for ages 5 to 19 years.43 Age was calculated as the difference between the date of measurement and the date of birth, which was obtained for all children from their school files. WAZ, HAZ, and BAZ were used as indicators for present and past nutritional status. A cutoff of less than 22 SDs was used to report underweight and stunting, whereas a cutoff of more than +2 SDs was used to report obesity.42 Dental Measurements Caries was assessed by using the decayed, missing, filled, teeth (primary teeth) (dmft) index (d = decay to cavitation, m = missing due to caries, filled = restoration, t = total number of primary teeth) and followed the WHO criteria and coding.44 Due to the age of the sample and the subsequent low prevalence of caries in permanent dentition, e618
the emphasis was on caries experience in the primary dentition. Caries was recorded at the cavitation level. Dental examinations of children were conducted in daylight by using a disposable dental mirror. No radiographs were taken. A trained dentist who had no previous knowledge about the study rationale conducted the clinical examinations. The reproducibility of clinical dental data was checked by reexamination of 51 (12%) children. The k score for caries measurements was 0.81, representing almost perfect agreement.45 Statistical Analyses The variables considered as covariates were selected on the basis of the scientific literature on the associations under study. Before constructing multiple regression models, correlations between the variables were checked with a correlation matrix. Accordingly,
the variables chosen and used in the multiple regressions were age, gender, parent’s educational levels, and number of teeth present. Differences in continuous outcomes such as differences in z scores of weight and height were assessed by using a t test for normally distributed independent data. Where continuous variables exhibited nonnormal distributions, the Mann-Whitney test was used instead. The Jonckheere-Terpstra test was used for testing differences between .2 means in nonparametric ordered data. Analysis of variance was carried out initially to study the association between dmft groups and HAZ, WAZ, and BAZ. We used analysis of covariance in the next step to further control for possible confounders. Means with 95% confidence intervals were calculated. All analyses were performed by using Stata 10.0 (StataCorp, College Station, TX).
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RESULTS Demographic Variables Four hundred and seventeen (95.6%) of the 436 eligible children were included. The mean age of the participants was 82.1 (65.8) months, and 42.0% were boys. In terms of parental education, 22.3% of fathers and 18.2% of mothers were educated to the university level or higher (Table 1). There is no accepted method for the assessment of socioeconomic position in Saudi Arabia. Therefore, gross national income per capita ($24 700 per year or $2058 per month) was considered in deciding the most appropriate categorization of children’s socioeconomic position.46 Because we wanted to include a low socioeconomic position group, we chose a considerably lower income (almost one-third less) than the mean national income per capita cutoff for that purpose. More specifically, children whose families had a monthly income ,50 000 Reyals (,$1333) were considered the low-income group (11.8%), those with a monthly income between
5000 and 10 000 Reyals ($$1332–$2663) were considered the middle-income group (46.5%), and those with a monthly income .10 000 Reyals (.$2663) were considered the high-income group (31.9%). Anthropometric Outcomes On the basis of the WHO reference values, 7.0% of children were determined to be underweight, 6.0% were stunted, 10.1% were overweight, and 9.4% were obese. Mean (6SD) HAZ, WAZ, and BAZ were 20.55 6 0.98, 20.31 6 1.39, and 20.01 6 1.4, respectively. Dental Caries Status The mean (6SD) number of primary teeth present was 16.2 6 2.9. The mean dmft was 5.7 6 4.2 teeth, and the median was 5.0 teeth (Table 2). Only 54 (12.9%) children were caries-free in their primary teeth, whereas 396 (95.2%) were caries-free in their permanent teeth. Untreated decay (d) accounted for 89.5% of the dmft; a mean of 5.1 of a dmft of 5.7 represented
untreated decay (d). Of the 363 (87.1% of the whole sample) with caries in the primary dentition, 286 (78.8%) had only unrestored caries, 9 (2.5%) had only fillings, and 68 (18.7%) had unrestored caries and fillings. Because there is no accepted classification for caries severity for this age group, 2 classifications were used to assess the inverse-graded association. First, the data were divided into 3 groups with comparable group sizes (tertiles); 28.5% of children had dmft in 0 to 2 teeth, 30.1% had dmft in 3 to 6 teeth, and 41.4% had dmft in $7 teeth. We also used a dmft variable with 4 categories. For that, caries-free children formed a distinct group and children with caries were divided into 3 groups with similar numbers of subjects (approximate tertiles): 12.9% of children were caries-free, 31.8% had dmft in 1 to 4 teeth, 28.9% had dmft in 5 to 8 teeth, and 26.3% had dmft in $9 teeth. Both classifications were used in the analysis to check for any differences (Table 3). Associations Between Caries Levels and WAZ, HAZ, and BAZ
TABLE 1 Sociodemographic Distribution Profiles of the Sample of Saudi Children Variable Gender Male Female Father’s educational level Cannot read or write Primary school Secondary school High school level University degree Above bachelor’s degree Missing data Mother’s educational level Cannot read or write Primary school Secondary school High school level University degree Above bachelor’s degree Missing data Family monthly income Low income: ,5000 Reyals (,$1332) Middle income: $5000–10 000 Reyals ($$1332–$2663) High income: .10 000 Reyals (.$2663) Missing data N = 417.
Frequency, N
Relative Frequency, %
175 242
42.0 58.0
5 31 102 150 72 21 36
1.2 7.4 24.5 36.0 17.3 5.0 8.6
31 80 97 95 75 1 38
7.4 19.2 23.3 22.8 18.0 0.2 9.1
49 194 133 41
11.8 46.5 31.9 9.8
Table 3 displays the results of multiple regression analyses showing the means of anthropometric indices by caries status groups, before and after adjustment for covariates (gender, age, father’s and mother’s educational levels, and number of teeth). Using dmft tertile classification, unadjusted mean HAZ scores were 20.32, 20.45, and 20.78 (P , .001). The unadjusted mean z scores were higher for each group with lower levels of caries. This strong association remained highly significant even after controlling for other covariates (adjusted mean HAZ scores were 20.32, 20.44, and 20.79; P , .001). A negative linear association was detected between unadjusted mean WAZ scores and caries categories (P , .001). After adjusting for confounders, mean WAZ scores were 0.12, 20.31, and
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TABLE 2 Distribution of the dmft, dt, mt, and ft Number of primary teeth dmft dt mt ft
Mean 6 SD
Median
Minimum
Maximum
16.2 6 2.9 5.7 6 4.2 5.1 6 4.1 0.2 6 0.8 0.4 6 1.0
17.0 5.0 5.0 0.0 0.0
5.0 0.0 0.0 0.0 0.0
20.0 20.0 16.0 9.0 9.0
N = 417. dt, decayed teeth; ft, filled teeth; mt, missing teeth.
20.62, respectively (P , .001). The same pattern of inverse linear relationship between caries categories was detected in BAZ after controlling for covariates. The adjusted mean BAZ values were 0.40, 20.12, and 20.21 (P = .001). To place the significance of the z score variation into perspective, for a 6-year-old girl in the highest caries group, the mean difference in height, weight, and BMI from WHO normal values was 3.3 cm, 1.2 kg, and 2.7 percentiles, respectively. There was a similar inverse-graded association between caries in both unadjusted and adjusted models for WAZ, HAZ, and BAZ scores when the analyses were repeated with the dmft second classification (caries-free and tertile classification). For each category with a higher prevalence of caries, the adjusted mean WAZ, HAZ, and BAZ scores were lower. This result indicates that the inverse-graded relationship was evident regardlessofthedmftclassificationused.
DISCUSSION This cross-sectional survey revealed a significant and robust inverse linear association between caries experience in 6- to 8-year-old children and HAZ, WAZ, and BAZ. The graded association remained highly significant after adjusting for demographic, dental, and social variables. Although some studies reported an inverse relationship between anthropometric outcomes and caries status,6,37,47 no previous study has reported an inverse-graded relationship. There are certain limitations when comparing the present study with e620
previous studies. First, all previous community-based studies either used categories such as underweight, overweight, and obesity6,8,26,27,31,32,36–38,48,49 or unstandardized categories such as obese and nonobese or at risk of underweight and normal weight depending on the distribution of their anthropometric measures,28,39 whereas the current study used all anthropometric outcomes as continuous variables. The reason for not using categories was that the objective was to study the relationship between caries and anthropometric measures by using all of the available data and examining the whole distribution rather than categorizing data and making assumptions about the direction of the relationship. Whereas categorization is sometimes needed, it undoubtedly results in loss of information.50 For example, GranvilleGarcia et al28 assessed the relationship between caries in obese and nonobese Brazilian children and found that there was no association between obesity and caries. On the other hand, they reported a significant association between high caries levels and not being obese. Due to their categorization and lack of information, it was difficult to assess whether the nonobese children were normal or underweight. Ngoenwiwatkul and Leela-adisorn 39 categorized their data into 2 groups, BMI ,15th percentile and BMI $15th percentile, because they had no underweight children and 45% of children were in the low-weight percentile category (5th percentile , BAZ , 15th percentile). This categorization made study comparisons difficult. In addition,
they could not assess linear associations in their data. A graded association between dmft and BMI was detected in a Turkish study6 in a similar age group and caries prevalence to the current study, but the authors did not control for confounders. Only tests for correlations were performed to show the presence of an inverse association between caries status and anthropometric outcomes. This inverted linear relationship between caries and BMI was also evident in an Australian longitudinal study.8 Interestingly, a Swedish study7 showed an inverted relationship between BMI categories (combined underweight and low-weight group, normal-weight group, and combined high-weight and obese group) and untreated caries (d) but not for decayed, extracted, filled, teeth (primary teeth) (deft) index. A possible explanation for the difference in findings for untreated decay (d) and deft may be that the inverted relationship exists only when untreated decay (d) accounts for a high proportion of the dmft. In the current study, untreated decay (d) accounted for almost 90% of the dmft. Therefore, the inverted relationship was also evident when dmft was used. This finding suggests that a high filling (f)-to-dmft ratio in some studies may have biased the results toward a positive relationship between dmft and a high BMI. Future studies should report the numbers of decayed teeth (d) and filled teeth (f). A second limitation in comparing our study with other studies is that most studies used different indices and definitions of caries. For example, the American Academy of Pediatric Dentistry criteria include noncavitated lesions in the definition of severe early childhood caries in young children, whereas the WHO criteria for caries include only cavitated lesions. Studies using different criteria will result in
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0.28 (20.11 to 0.67) 0.20 (20.05 to 0.45) 20.17 (20.43 to 0.09) 20.24 (20.52 to 0.03) .01
0.25 (20.13 to 0.65) 0.17 (20.08 to 0.42) 20.15 (20.41 to 0.11) 20.22 (20.49 to 0.06) .02
different prevalence rates and cannot be compared easily. Even when 1 caries definition was used, different indices were reported. For example, some studies reported dmft, whereas others reported dmfs (decayed, missing, filled, surfaces [primary teeth]). Third, studies had differing levels and various methods of assessing anthropometric measures. Most studies that assessed the relationship between caries and malnutrition in children depended solely on BMI4,7,31,32,36 and did not report other anthropometric outcomes.
N = 417. CI, confidence interval. a Analysis of variance. b Analysis of covariance (adjusted for gender, age, father’s and mother’s educational levels, and number of teeth present).
20.24 (20.50 to 20.01) 20.37 (20.54 to 20.21) 20.68 (20.85 to 20.51) 20.77 (20.95 to 20.59) ,.001 12.9 31.8 28.9 26.3
0.27 (20.53 to 20.01) 20.37 (20.53 to 20.20) 20.68 (20.85 to 20.50) 20.77 (20.95 to 20.59) ,.001
0.05 (20.31 to 0.42) 20.05 (20.28 to 0.18) 20.50 (20.75 to 20.25) 20.62 (20.88 to 20.38) ,.001
0.05 (20.31 to 0.48) 20.06 (20.30 to 0.16) 20.49 (20.74 to 20.25) 20.61 (20.86 to 20.35) .001
0.40 (0.13 to 0.66) 20.12 (20.37 to 0.13) 20.21 (20.43 to 0.01) .001 0.44 (0.18 to 0.71) 20.17 (20.43 to 0.08) 20.21 (20.42 to 0.01) ,.001 0.12 (20.13 to 0.37) 20.31 (20.55 to 20.08) 20.62 (20.82 to 20.42) ,0.001 0.14 (20.10 to 0.39) 20.35 (20.59 to 20.12) 20.61 (20.81 to 20.40) ,.001 20.32 (20.49 to 20.14) 20.44 (20.60 to 20.27) 20.79 (20.94 to 20.66) ,.001 20.32 (20.50 to 20.15) 20.45 (20.62 to 20.28) 20.78 (20.92 to 20.63) ,.001 28.5 30.1 41.4
Unadjusted Mean (95% CI)
Adjusted Mean (95% CI)
b
Percentage Variable
TABLE 3 Association Between Anthropometric Outcomes and dmft
Tertile classification dmft #2 (lowest-caries group) dmft = 3–6 dmft $7 (highest-caries group) P for trend Caries-free and tertile classification dmft = 0 (caries-free group) dmft = 1–4 dmft = 5–8 dmft $9 (highest-caries group) P for trend
Unadjusted Mean (95% CI)a Adjusted Mean (95% CI)b a a
Unadjusted Mean (95% CI)
WHO WAZ WHO HAZ
Adjusted Mean (95% CI)
b
WHO BAZ
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Fourth, in the current study, the WHO 2007 growth references were used to assess height and weight. These references have not been applied in the majority of previous dental studies and therefore comparison of their results with the current study should be made with caution. One study6 did use these references, and their results agree with those of the current study. Fifth, some studies did not provide any evidence on the reliability of clinical measures and no study indicated the time when the child was weighed or took into account the child’s mealtimes. Sixth, the samples used in some studies included different age groups and children from different social and ethnic backgrounds. For the reasons outlined above, there are doubts whether the apparently contradictory findings were due to methodologic inconsistencies or are a true reflection of differences. Due to the cross-sectional study design, definitive information about causeand-effect relationships cannot be determined. Another limitation of the current study is that the sample was not representative of Saudi children. Consequently, it is difficult to extrapolate findings to the Saudi child population. However, our aim was not to have a nationally representative sample but to assess the association between caries and anthropometric outcomes in
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a child population with high levels of untreated caries. A recent systematic review revealed that many studies have failed to include samples representing the full range of BMI categories.51 In that respect, a strength of this study is that the sample represented a good range of BMI values, which included both under- and overweight children with different levels of caries experience. Although several demographic and socioeconomic variables were controlled for, other potential confounders such as nutrition, low birth weight, and appetite were not assessed. All of these uncontrolled confounders could have biased our results. In addition, due to the use of WHO criteria, which include only cavitated lesions, the prevalence of caries in this study may have been underestimated. However, these are standard epidemiologic criteria for caries detection and have been used worldwide. Furthermore, missing data could have affected our findings. To overcome that possibility, missing data in social variables, such as parents’
educational levels, were coded as a special category and were not excluded from analysis, and missing data were therefore kept to a minimum. By demonstrating the inverse-graded relationship between caries and children’s height and weight, our results have considerable public health implications, indicating the need for health promotion programs to address both oral and general health in high-caries populations at an early age. Severe caries is strongly associated with anemia and iron deficiency and thereby may be a contributing factor for poor growth in young children.14 Malnutrition and caries can be addressed efficiently early in life. Therefore, primary health care providers and pediatricians have the potential to play an important role in actively participating in health promotion interventions with young children. In terms of future research, longitudinal studies are needed to determine whether there is a cause-and-effect relationship between caries levels and poor growth. Such a study would benefit
from adequate adjustment for confounding variables and from the use of continuous outcomes in addition to categories of malnutrition.
CONCLUSIONS There was an inverse-graded association between all anthropometric outcomes and caries levels in 6- to 8year-old Saudi children. Children at each higher level of caries had significantly lower height and weight outcomes than those with lower caries levels. Future longitudinal studies can help determine whether there is a cause-and-effect relationship between caries levels and poor growth.
ACKNOWLEDGMENTS We thank the sponsor, King Fahad Armed Forces Hospital, and the schools, children, and their families who participated. We also thank the study investigators, especially Dr Alya Altaf and Miss Manal Alamri.
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pulpal pathogenesis. Infect Immun. 2000;68 (12):6785–6789 Plitnick LM, Banas JA, Jelley-Gibbs DM, et al. Inhibition of interleukin-2 by a Grampositive bacterium, Streptococcus mutans. Immunology. 1998;95(4):522–528 Means RT Jr. Recent developments in the anemia of chronic disease. Curr Hematol Rep. 2003;2(2):116–121 Barton BE. IL-6: insights into novel biological activities. Clin Immunol Immunopathol. 1997;85(1):16–20 Stephensen CB. Burden of infection on growth failure. J Nutr. 1999;129(2S suppl): 534S–538S Exton MS. Infection-induced anorexia: active host defence strategy. Appetite. 1997;29(3): 369–383 Kelley KW, Bluthé R-M, Dantzer R, et al. Cytokine-induced sickness behavior. Brain Behav Immun. 2003;17(suppl 1):S112–S118 Plata-Salamán CR. Anorexia during acute and chronic disease. Nutrition. 1996;12(2): 69–78 Alkarimi HA, Watt RG, Pikhart H, Jawadi AH, Sheiham A, Tsakos G. Impact of treating dental caries on schoolchildren’s anthropometric, dental, satisfaction and appetite outcomes: a randomized controlled trial. BMC Public Health. 2012;12(1):706 Phillip M, Hershkovitz E, Rosenblum H, et al. Serum insulin-like growth factors I and II are not affected by undernutrition in children with nonorganic failure to thrive. Horm Res. 1998;49(2):76–79 Hilgers KK, Kinane DE, Scheetz JP. Association between childhood obesity and smooth-surface caries in posterior teeth: a preliminary study. Pediatr Dent. 2006;28 (1):23–28 Chen W, Chen P, Chen SC, Shih WT, Hu HC. Lack of association between obesity and dental caries in three-year-old children. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi. 1998;39(2):109–111 Granville-Garcia AF, de Menezes VA, de Lira PI, Ferreira JM, Leite-Cavalcanti A. Obesity and dental caries among preschool children in Brazil. Rev Salud Publica (Bogota). 2008;10(5):788–795 Hayden C, Bowler JO, Chambers S, et al. Obesity and dental caries in children:
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a systematic review and meta-analysis. Community Dent Oral Epidemiol. 2013;41(4): 289–308 Kantovitz KR, Pascon FM, Rontani RMP, Gavião MBD. Obesity and dental caries— a systematic review. Oral Health Prev Dent. 2006;4(2):137–144 Sharma A, Hegde AM. Relationship between body mass index, caries experience and dietary preferences in children. J Clin Pediatr Dent. 2009;34(1):49–52 Willerhausen B, Blettner M, Kasaj A, Hohenfellner K. Association between body mass index and dental health in 1,290 children of elementary schools in a German city. Clin Oral Investig. 2007;11(3): 195–200 Thomas CW, Primosch RE. Changes in incremental weight and well-being of children with rampant caries following complete dental rehabilitation. Pediatr Dent. 2002;24(2):109–113 Malek Mohammadi T, Wright CM, Kay EJ. Childhood growth and dental caries. Community Dent Health. 2009;26(1):38–42 van Gemert-Schriks MC, van Amerongen EW, Aartman IHA, Wennink JMB, Ten Cate JM, de Soet JJ. The influence of dental caries on body growth in prepubertal children. Clin Oral Investig. 2011;15(2):141– 149 Pinto A, Kim S, Wadenya R, Rosenberg H. Is there an association between weight and dental caries among pediatric patients in an urban dental school? A correlation study. J Dent Educ. 2007;71(11):1435–1440 Macek MD, Mitola DJ. Exploring the association between overweight and dental caries among US children. Pediatr Dent. 2006;28(4):375–380 Hong L, Ahmed A, McCunniff M, Overman P, Mathew M. Obesity and dental caries in children aged 2-6 years in the United States: National Health and Nutrition Examination Survey 1999-2002. J Public Health Dent. 2008;68(4):227–233 Ngoenwiwatkul Y, Leela-adisorn N. Effects of dental caries on nutritional status among first-grade primary school children. Asia Pac J Public Health. 2009;21(2):177–183 Al-Malik MI, Rehbini YA. Prevalence of dental caries, severity, and pattern in age 6 to
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7-year-old children in a selected community in Saudi Arabia. J Contemp Dent Pract. 2006;7(2):46–54 Cogill B. Anthropometric Indicators Measurement Guide. Food and Nutrition Technical Assistance Project. Washington, DC: Academy for Educational Development; 2003 de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85(9):660–667 World Health Organization. AnthroPlus 2007: software for the global application of the WHO Reference 2007 for 5-19 years to monitor the growth of school-age children and adolescents. Geneva, Switzerland: World Health Organization; 2007. Available at: www. who.int/growthref/en/. Accessed September 24, 2009 World Health Organization. Oral Health Surveys: Basic Methods. Geneva, Switzerland: World Health Organization; 1997 Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas. 1960;20 (1):37–46 World Health Organization. Saudi Arabia. Available at: www.who.int/countries/sau/ en/. Accessed July 22, 2013 Pine CM, Harris RV, Burnside G, Merrett MCW. An investigation of the relationship between untreated decayed teeth and dental sepsis in 5-year-old children. Br Dent J. 2006; 200(1):45–47; discussion 29 Vania A, Parisella V, Capasso F, et al. Early childhood caries underweight or overweight, that is the question. Eur J Paediatr Dent. 2011;12(4):231–235 Mojarad F, Maybodi MH. Association between dental caries and body mass index among Hamedan elementary school children in 2009. J Dent (Tehran). 2011;8(4): 170–177 Owen SV, Froman RD. Why carve up your continuous data? Res Nurs Health. 2005;28 (6):496–503 Hooley M, Skouteris H, Boganin C, Satur J, Kilpatrick N. Body mass index and dental caries in children and adolescents: a systematic review of literature published 2004 to 2011. Syst Rev. 2012;1(1):57
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Dental Caries and Growth in School-Age Children Heba A. Alkarimi, Richard G. Watt, Hynek Pikhart, Aubrey Sheiham and Georgios Tsakos Pediatrics 2014;133;e616; originally published online February 17, 2014; DOI: 10.1542/peds.2013-0846 Updated Information & Services
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
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The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/133/3/e616.full.html
PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
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Dental Caries and Growth in School-Age Children WHAT’S KNOWN ON THIS SUBJECT: There is conflicting evidence about the relationship between dental caries in primary teeth and children’s height and weight.
AUTHORS: Heba A. Alkarimi, MSc, PhD,a,b Richard G. Watt, MSc, PhD,b Hynek Pikhart, MSc, PhD,b Aubrey Sheiham, BDS, PhD,b and Georgios Tsakos, MSc, PhDb aKing
WHAT THIS STUDY ADDS: Findings reveal an inverse linear association between caries levels and children’s height and weight. The findings take the argument beyond the presence or absence of an association and provide a better understanding of the pattern of this association.
abstract BACKGROUND AND OBJECTIVE: Dental caries in young children is commonly untreated and represents a public health problem. Dental caries in children is reported to affect their anthropometric outcomes, but the evidence is conflicting. Some studies found no association, whereas others found that caries was associated with underweight or overweight. The objective was to assess the relationship between dental caries status and height and weight in 6- to 8-year-old Saudi children with high caries prevalence. METHODS: This study was a cross-sectional survey in schoolchildren aged 6 to 8 years attending military primary schools in Jeddah, Saudi Arabia. Caries status was assessed by using the dmft (decayed, missing, filled, teeth [primary teeth]) index. Height and weight were assessed by using z scores of height-for-age (HAZ), weight-for-age (WAZ), and BMI-for-age (BAZ) calculated by World Health Organization standardized procedures. Relationships between caries and HAZ, WAZ, and BAZ were assessed by using regression models. RESULTS: A total of 417 of the 436 eligible schoolchildren with complete data were included, with a response rate of 95.6%. Their mean dmft index was 5.7 6 4.2. There was an inverse linear relationship between caries status and children’s HAZ, WAZ, and BAZ and significantly lower anthropometric outcomes for children at each consecutive group with higher levels of caries. The associations remained significant after adjusting for dental, social, and demographic variables.
Fahad Armed Forces Hospital, Jeddah, Saudi Arabia; and Department of Epidemiology and Public Health University College London, London, United Kingdom bResearch
KEY WORDS height, weight, BMI, children, caries ABBREVIATIONS BAZ—BMI-for-age dmft—decayed, missing, filled, teeth (primary teeth) HAZ—height-for-age WAZ—weight-for-age WHO—World Health Organization Dr Alkarimi conceptualized and designed the study, carried out the analyses, and drafted the initial manuscript; Drs Watt and Sheiham conceptualized and designed the study and reviewed and revised the manuscript; Dr Pikhart contributed to the study design and data analysis and interpretation and reviewed and revised the manuscript; Dr Tsakos conceptualized and designed the study, contributed to data analysis and interpretation, and reviewed and revised the manuscript; and all authors approved the final manuscript as submitted. www.pediatrics.org/cgi/doi/10.1542/peds.2013-0846 doi:10.1542/peds.2013-0846 Accepted for publication Dec 17, 2013 Address correspondence to Heba Alkarimi, MSc, PhD, King Fahad Armed Forces Hospital (KFAFH), PO Box 54146, Jeddah, 21514, Saudi Arabia. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2014 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: Funded by the Saudi Ministry of Defense, King Fahad Armed Forces Hospital. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
CONCLUSIONS: The inverse linear association between dental caries and all anthropometric outcomes suggests that higher levels of untreated caries are associated with poorer growth in Saudi schoolchildren. Pediatrics 2014;133:e616–e623
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There is increased interest in the relationship between caries and growth in young children and mechanisms whereby caries may affect growth. Evidence linking caries in primary teeth and children’s anthropometric outcomes in cross-sectional studies is contradictory in terms of both the presence and the direction of the association. Some studies report a relationship between caries and poor growth.1–9 Two theories may explain this relationship (Fig 1). The first theory is that the direct impact of extensive untreated caries and associated pain and inflammation on the child’s ability to eat may result in undernutrition and growth impairment.1,10–14 The second theory includes the indirect effects of untreated caries and different body responses to chronic dental infection. Three mechanisms are suggested. The first concerns immune responses. Infected dental pulp may affect immunity and erythropoiesis,15–17 which may result in anemia18 and influence bone remodeling,19,20 sleep patterns,21,22 and food intake.23 This mechanism is supported by results of a randomized controlled trial showing that treatment of severe caries in children aged 6 to 7 years significantly improved their appetite.24 The second mechanism is related to endocrine responses. The interruption of slowwave sleep due to pain and infection may lead to impairment of growth hormone secretion.25 The third mechanism is linked to metabolic responses. Infections and related inflammation might result in micronutrient undernutrition through increasing energy expenditure and metabolic demands and impaired nutrient absorption.20 In contrast to the studies reporting a relationship between caries and poor growth, some studies did not find any relationship between anthropometric outcomes and caries26–29 or reported that caries is related to overweight.30–32
This inconsistency is also observed in findings from randomized controlled trials and nonrandom longitudinal studies.9,11,24,33–35 These inconsistent associations could be due to methodologic limitations, different caries definitions and detection methods, relying only on BMI, and using unadjusted formulas to calculate BMI rather than the age- and gender-adjusted World Health Organization (WHO)–recommended growth references.4,26,32,36–38 Another limitation is the failure to include the full range of BMI categories in the sample.37,38 In addition, most studies only focused on 1 direction of the association, either underweight or overweight, ignoring other possibilities.4,26,28,37–39 Interestingly, a recent systematic review showed a significant association between obesity and caries when BMIfor-age (BAZ) centiles were reported and nonsignificant findings when z scores or nonstandardized scales were reported.29 To date, no study has examined the relationship between caries and anthropometric outcomes in young children with high levels of untreated caries using height and weight as continuous variables and where no cutoff points for the diagnosis of underweight and overweight are used. Therefore, a study was conducted with the objective of assessing the nature of the relationship between different levels of caries and height and weight among 6- to 8-year-old Saudi schoolchildren. No assumptions were made on the direction of this association.
METHODS The sample consisted of all schoolchildren aged 6 to 8 years in the firstyear class (grade 1) of all military primary schools inJeddah, SaudiArabia. Children with parasitic infections at the time of the survey and children whose caregivers did not give consent were excluded. Children of military
personnel were selected because they had the highest prevalence of caries in Saudi Arabia.40 Parents were asked to complete a sociodemographic and health status questionnaire. A pilot study was conducted in 55 randomly selected children to test the feasibility of all clinical examinations. The research was approved, managed, and monitored by the Research and Ethics Committee of the King Fahad Armed Forces Hospital. Parental permission was obtained from the child’s legal caregivers. Measurements Anthropometric Measurements Anthropometric measurements were performed by using the Food and Nutrition Anthropometric Indictors Measurement Guide.41 A skilled nurse, blinded to the child’s dental status, carried out all anthropometric measurements. Measurements for height and weight were made to the nearest 0.1 cm and 0.1 kg, respectively. All anthropometric measures were performed in children without shoes and wearing light clothes. Height was measured by using a portable Harpenden pocket stadiometer (Chasmors Ltd, London, United Kingdom). Weight was measured by using a precalibrated digital Seca scale (model 767; Seca GmbH, Hamburg, Germany). All children were weighed at the same time of day (7:30–8:50 AM) and in the same relation to their eating time (before morning break). Three readings for both height and weight were taken for each child. The median of these readings was used for the analysis. Height and weight were assessed by using the z scores of height-for-age (HAZ), weight-for-age (WAZ), and BAZ.42 The calculation of z scores for height, weight, and BMI was based on the international reference standards for the assessment of nutritional status for a specific age and gender and were automatically
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FIGURE 1 Proposed mechanisms linking severe dental caries and dental pain and infections with height and weight in young children.
managed by using the WHO AnthroPlus software, which holds the WHO Reference 2007 for ages 5 to 19 years.43 Age was calculated as the difference between the date of measurement and the date of birth, which was obtained for all children from their school files. WAZ, HAZ, and BAZ were used as indicators for present and past nutritional status. A cutoff of less than 22 SDs was used to report underweight and stunting, whereas a cutoff of more than +2 SDs was used to report obesity.42 Dental Measurements Caries was assessed by using the decayed, missing, filled, teeth (primary teeth) (dmft) index (d = decay to cavitation, m = missing due to caries, filled = restoration, t = total number of primary teeth) and followed the WHO criteria and coding.44 Due to the age of the sample and the subsequent low prevalence of caries in permanent dentition, e618
the emphasis was on caries experience in the primary dentition. Caries was recorded at the cavitation level. Dental examinations of children were conducted in daylight by using a disposable dental mirror. No radiographs were taken. A trained dentist who had no previous knowledge about the study rationale conducted the clinical examinations. The reproducibility of clinical dental data was checked by reexamination of 51 (12%) children. The k score for caries measurements was 0.81, representing almost perfect agreement.45 Statistical Analyses The variables considered as covariates were selected on the basis of the scientific literature on the associations under study. Before constructing multiple regression models, correlations between the variables were checked with a correlation matrix. Accordingly,
the variables chosen and used in the multiple regressions were age, gender, parent’s educational levels, and number of teeth present. Differences in continuous outcomes such as differences in z scores of weight and height were assessed by using a t test for normally distributed independent data. Where continuous variables exhibited nonnormal distributions, the Mann-Whitney test was used instead. The Jonckheere-Terpstra test was used for testing differences between .2 means in nonparametric ordered data. Analysis of variance was carried out initially to study the association between dmft groups and HAZ, WAZ, and BAZ. We used analysis of covariance in the next step to further control for possible confounders. Means with 95% confidence intervals were calculated. All analyses were performed by using Stata 10.0 (StataCorp, College Station, TX).
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RESULTS Demographic Variables Four hundred and seventeen (95.6%) of the 436 eligible children were included. The mean age of the participants was 82.1 (65.8) months, and 42.0% were boys. In terms of parental education, 22.3% of fathers and 18.2% of mothers were educated to the university level or higher (Table 1). There is no accepted method for the assessment of socioeconomic position in Saudi Arabia. Therefore, gross national income per capita ($24 700 per year or $2058 per month) was considered in deciding the most appropriate categorization of children’s socioeconomic position.46 Because we wanted to include a low socioeconomic position group, we chose a considerably lower income (almost one-third less) than the mean national income per capita cutoff for that purpose. More specifically, children whose families had a monthly income ,50 000 Reyals (,$1333) were considered the low-income group (11.8%), those with a monthly income between
5000 and 10 000 Reyals ($$1332–$2663) were considered the middle-income group (46.5%), and those with a monthly income .10 000 Reyals (.$2663) were considered the high-income group (31.9%). Anthropometric Outcomes On the basis of the WHO reference values, 7.0% of children were determined to be underweight, 6.0% were stunted, 10.1% were overweight, and 9.4% were obese. Mean (6SD) HAZ, WAZ, and BAZ were 20.55 6 0.98, 20.31 6 1.39, and 20.01 6 1.4, respectively. Dental Caries Status The mean (6SD) number of primary teeth present was 16.2 6 2.9. The mean dmft was 5.7 6 4.2 teeth, and the median was 5.0 teeth (Table 2). Only 54 (12.9%) children were caries-free in their primary teeth, whereas 396 (95.2%) were caries-free in their permanent teeth. Untreated decay (d) accounted for 89.5% of the dmft; a mean of 5.1 of a dmft of 5.7 represented
untreated decay (d). Of the 363 (87.1% of the whole sample) with caries in the primary dentition, 286 (78.8%) had only unrestored caries, 9 (2.5%) had only fillings, and 68 (18.7%) had unrestored caries and fillings. Because there is no accepted classification for caries severity for this age group, 2 classifications were used to assess the inverse-graded association. First, the data were divided into 3 groups with comparable group sizes (tertiles); 28.5% of children had dmft in 0 to 2 teeth, 30.1% had dmft in 3 to 6 teeth, and 41.4% had dmft in $7 teeth. We also used a dmft variable with 4 categories. For that, caries-free children formed a distinct group and children with caries were divided into 3 groups with similar numbers of subjects (approximate tertiles): 12.9% of children were caries-free, 31.8% had dmft in 1 to 4 teeth, 28.9% had dmft in 5 to 8 teeth, and 26.3% had dmft in $9 teeth. Both classifications were used in the analysis to check for any differences (Table 3). Associations Between Caries Levels and WAZ, HAZ, and BAZ
TABLE 1 Sociodemographic Distribution Profiles of the Sample of Saudi Children Variable Gender Male Female Father’s educational level Cannot read or write Primary school Secondary school High school level University degree Above bachelor’s degree Missing data Mother’s educational level Cannot read or write Primary school Secondary school High school level University degree Above bachelor’s degree Missing data Family monthly income Low income: ,5000 Reyals (,$1332) Middle income: $5000–10 000 Reyals ($$1332–$2663) High income: .10 000 Reyals (.$2663) Missing data N = 417.
Frequency, N
Relative Frequency, %
175 242
42.0 58.0
5 31 102 150 72 21 36
1.2 7.4 24.5 36.0 17.3 5.0 8.6
31 80 97 95 75 1 38
7.4 19.2 23.3 22.8 18.0 0.2 9.1
49 194 133 41
11.8 46.5 31.9 9.8
Table 3 displays the results of multiple regression analyses showing the means of anthropometric indices by caries status groups, before and after adjustment for covariates (gender, age, father’s and mother’s educational levels, and number of teeth). Using dmft tertile classification, unadjusted mean HAZ scores were 20.32, 20.45, and 20.78 (P , .001). The unadjusted mean z scores were higher for each group with lower levels of caries. This strong association remained highly significant even after controlling for other covariates (adjusted mean HAZ scores were 20.32, 20.44, and 20.79; P , .001). A negative linear association was detected between unadjusted mean WAZ scores and caries categories (P , .001). After adjusting for confounders, mean WAZ scores were 0.12, 20.31, and
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TABLE 2 Distribution of the dmft, dt, mt, and ft Number of primary teeth dmft dt mt ft
Mean 6 SD
Median
Minimum
Maximum
16.2 6 2.9 5.7 6 4.2 5.1 6 4.1 0.2 6 0.8 0.4 6 1.0
17.0 5.0 5.0 0.0 0.0
5.0 0.0 0.0 0.0 0.0
20.0 20.0 16.0 9.0 9.0
N = 417. dt, decayed teeth; ft, filled teeth; mt, missing teeth.
20.62, respectively (P , .001). The same pattern of inverse linear relationship between caries categories was detected in BAZ after controlling for covariates. The adjusted mean BAZ values were 0.40, 20.12, and 20.21 (P = .001). To place the significance of the z score variation into perspective, for a 6-year-old girl in the highest caries group, the mean difference in height, weight, and BMI from WHO normal values was 3.3 cm, 1.2 kg, and 2.7 percentiles, respectively. There was a similar inverse-graded association between caries in both unadjusted and adjusted models for WAZ, HAZ, and BAZ scores when the analyses were repeated with the dmft second classification (caries-free and tertile classification). For each category with a higher prevalence of caries, the adjusted mean WAZ, HAZ, and BAZ scores were lower. This result indicates that the inverse-graded relationship was evident regardlessofthedmftclassificationused.
DISCUSSION This cross-sectional survey revealed a significant and robust inverse linear association between caries experience in 6- to 8-year-old children and HAZ, WAZ, and BAZ. The graded association remained highly significant after adjusting for demographic, dental, and social variables. Although some studies reported an inverse relationship between anthropometric outcomes and caries status,6,37,47 no previous study has reported an inverse-graded relationship. There are certain limitations when comparing the present study with e620
previous studies. First, all previous community-based studies either used categories such as underweight, overweight, and obesity6,8,26,27,31,32,36–38,48,49 or unstandardized categories such as obese and nonobese or at risk of underweight and normal weight depending on the distribution of their anthropometric measures,28,39 whereas the current study used all anthropometric outcomes as continuous variables. The reason for not using categories was that the objective was to study the relationship between caries and anthropometric measures by using all of the available data and examining the whole distribution rather than categorizing data and making assumptions about the direction of the relationship. Whereas categorization is sometimes needed, it undoubtedly results in loss of information.50 For example, GranvilleGarcia et al28 assessed the relationship between caries in obese and nonobese Brazilian children and found that there was no association between obesity and caries. On the other hand, they reported a significant association between high caries levels and not being obese. Due to their categorization and lack of information, it was difficult to assess whether the nonobese children were normal or underweight. Ngoenwiwatkul and Leela-adisorn 39 categorized their data into 2 groups, BMI ,15th percentile and BMI $15th percentile, because they had no underweight children and 45% of children were in the low-weight percentile category (5th percentile , BAZ , 15th percentile). This categorization made study comparisons difficult. In addition,
they could not assess linear associations in their data. A graded association between dmft and BMI was detected in a Turkish study6 in a similar age group and caries prevalence to the current study, but the authors did not control for confounders. Only tests for correlations were performed to show the presence of an inverse association between caries status and anthropometric outcomes. This inverted linear relationship between caries and BMI was also evident in an Australian longitudinal study.8 Interestingly, a Swedish study7 showed an inverted relationship between BMI categories (combined underweight and low-weight group, normal-weight group, and combined high-weight and obese group) and untreated caries (d) but not for decayed, extracted, filled, teeth (primary teeth) (deft) index. A possible explanation for the difference in findings for untreated decay (d) and deft may be that the inverted relationship exists only when untreated decay (d) accounts for a high proportion of the dmft. In the current study, untreated decay (d) accounted for almost 90% of the dmft. Therefore, the inverted relationship was also evident when dmft was used. This finding suggests that a high filling (f)-to-dmft ratio in some studies may have biased the results toward a positive relationship between dmft and a high BMI. Future studies should report the numbers of decayed teeth (d) and filled teeth (f). A second limitation in comparing our study with other studies is that most studies used different indices and definitions of caries. For example, the American Academy of Pediatric Dentistry criteria include noncavitated lesions in the definition of severe early childhood caries in young children, whereas the WHO criteria for caries include only cavitated lesions. Studies using different criteria will result in
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0.28 (20.11 to 0.67) 0.20 (20.05 to 0.45) 20.17 (20.43 to 0.09) 20.24 (20.52 to 0.03) .01
0.25 (20.13 to 0.65) 0.17 (20.08 to 0.42) 20.15 (20.41 to 0.11) 20.22 (20.49 to 0.06) .02
different prevalence rates and cannot be compared easily. Even when 1 caries definition was used, different indices were reported. For example, some studies reported dmft, whereas others reported dmfs (decayed, missing, filled, surfaces [primary teeth]). Third, studies had differing levels and various methods of assessing anthropometric measures. Most studies that assessed the relationship between caries and malnutrition in children depended solely on BMI4,7,31,32,36 and did not report other anthropometric outcomes.
N = 417. CI, confidence interval. a Analysis of variance. b Analysis of covariance (adjusted for gender, age, father’s and mother’s educational levels, and number of teeth present).
20.24 (20.50 to 20.01) 20.37 (20.54 to 20.21) 20.68 (20.85 to 20.51) 20.77 (20.95 to 20.59) ,.001 12.9 31.8 28.9 26.3
0.27 (20.53 to 20.01) 20.37 (20.53 to 20.20) 20.68 (20.85 to 20.50) 20.77 (20.95 to 20.59) ,.001
0.05 (20.31 to 0.42) 20.05 (20.28 to 0.18) 20.50 (20.75 to 20.25) 20.62 (20.88 to 20.38) ,.001
0.05 (20.31 to 0.48) 20.06 (20.30 to 0.16) 20.49 (20.74 to 20.25) 20.61 (20.86 to 20.35) .001
0.40 (0.13 to 0.66) 20.12 (20.37 to 0.13) 20.21 (20.43 to 0.01) .001 0.44 (0.18 to 0.71) 20.17 (20.43 to 0.08) 20.21 (20.42 to 0.01) ,.001 0.12 (20.13 to 0.37) 20.31 (20.55 to 20.08) 20.62 (20.82 to 20.42) ,0.001 0.14 (20.10 to 0.39) 20.35 (20.59 to 20.12) 20.61 (20.81 to 20.40) ,.001 20.32 (20.49 to 20.14) 20.44 (20.60 to 20.27) 20.79 (20.94 to 20.66) ,.001 20.32 (20.50 to 20.15) 20.45 (20.62 to 20.28) 20.78 (20.92 to 20.63) ,.001 28.5 30.1 41.4
Unadjusted Mean (95% CI)
Adjusted Mean (95% CI)
b
Percentage Variable
TABLE 3 Association Between Anthropometric Outcomes and dmft
Tertile classification dmft #2 (lowest-caries group) dmft = 3–6 dmft $7 (highest-caries group) P for trend Caries-free and tertile classification dmft = 0 (caries-free group) dmft = 1–4 dmft = 5–8 dmft $9 (highest-caries group) P for trend
Unadjusted Mean (95% CI)a Adjusted Mean (95% CI)b a a
Unadjusted Mean (95% CI)
WHO WAZ WHO HAZ
Adjusted Mean (95% CI)
b
WHO BAZ
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Fourth, in the current study, the WHO 2007 growth references were used to assess height and weight. These references have not been applied in the majority of previous dental studies and therefore comparison of their results with the current study should be made with caution. One study6 did use these references, and their results agree with those of the current study. Fifth, some studies did not provide any evidence on the reliability of clinical measures and no study indicated the time when the child was weighed or took into account the child’s mealtimes. Sixth, the samples used in some studies included different age groups and children from different social and ethnic backgrounds. For the reasons outlined above, there are doubts whether the apparently contradictory findings were due to methodologic inconsistencies or are a true reflection of differences. Due to the cross-sectional study design, definitive information about causeand-effect relationships cannot be determined. Another limitation of the current study is that the sample was not representative of Saudi children. Consequently, it is difficult to extrapolate findings to the Saudi child population. However, our aim was not to have a nationally representative sample but to assess the association between caries and anthropometric outcomes in
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a child population with high levels of untreated caries. A recent systematic review revealed that many studies have failed to include samples representing the full range of BMI categories.51 In that respect, a strength of this study is that the sample represented a good range of BMI values, which included both under- and overweight children with different levels of caries experience. Although several demographic and socioeconomic variables were controlled for, other potential confounders such as nutrition, low birth weight, and appetite were not assessed. All of these uncontrolled confounders could have biased our results. In addition, due to the use of WHO criteria, which include only cavitated lesions, the prevalence of caries in this study may have been underestimated. However, these are standard epidemiologic criteria for caries detection and have been used worldwide. Furthermore, missing data could have affected our findings. To overcome that possibility, missing data in social variables, such as parents’
educational levels, were coded as a special category and were not excluded from analysis, and missing data were therefore kept to a minimum. By demonstrating the inverse-graded relationship between caries and children’s height and weight, our results have considerable public health implications, indicating the need for health promotion programs to address both oral and general health in high-caries populations at an early age. Severe caries is strongly associated with anemia and iron deficiency and thereby may be a contributing factor for poor growth in young children.14 Malnutrition and caries can be addressed efficiently early in life. Therefore, primary health care providers and pediatricians have the potential to play an important role in actively participating in health promotion interventions with young children. In terms of future research, longitudinal studies are needed to determine whether there is a cause-and-effect relationship between caries levels and poor growth. Such a study would benefit
from adequate adjustment for confounding variables and from the use of continuous outcomes in addition to categories of malnutrition.
CONCLUSIONS There was an inverse-graded association between all anthropometric outcomes and caries levels in 6- to 8year-old Saudi children. Children at each higher level of caries had significantly lower height and weight outcomes than those with lower caries levels. Future longitudinal studies can help determine whether there is a cause-and-effect relationship between caries levels and poor growth.
ACKNOWLEDGMENTS We thank the sponsor, King Fahad Armed Forces Hospital, and the schools, children, and their families who participated. We also thank the study investigators, especially Dr Alya Altaf and Miss Manal Alamri.
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Dental Caries and Growth in School-Age Children Heba A. Alkarimi, Richard G. Watt, Hynek Pikhart, Aubrey Sheiham and Georgios Tsakos Pediatrics 2014;133;e616; originally published online February 17, 2014; DOI: 10.1542/peds.2013-0846 Updated Information & Services
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